Serially Homologous Research Articles

Anatomical Network Comparison of Human Upper and Lower, Newborn and Adult, and Normal and Abnormal Limbs, with Notes on Development, Pathology and Limb Serial Homology vs. Homoplasy.

How do the various anatomical parts (modules) of the animal body evolve into very different integrated forms (integration) yet still function properly without decreasing the individual’s survival? This long-standing question remains unanswered for multiple reasons, including lack of consensus about conceptual definitions and approaches, as well as a reasonable bias toward the study of hard tissues over soft tissues. A major difficulty concerns the non-trivial technical hurdles of addressing this problem, specifically the lack of quantitative tools to quantify and compare variation across multiple disparate anatomical parts and tissue types. In this paper we apply for the first time a powerful new quantitative tool, Anatomical Network Analysis (AnNA), to examine and compare in detail the musculoskeletal modularity and integration of normal and abnormal human upper and lower limbs. In contrast to other morphological methods, the strength of AnNA is that it allows efficient and direct empirical comparisons among body parts with even vastly different architectures (e.g. upper and lower limbs) and diverse or complex tissue composition (e.g. bones, cartilages and muscles), by quantifying the spatial organization of these parts—their topological patterns relative to each other—using tools borrowed from network theory. Our results reveal similarities between the skeletal networks of the normal newborn/adult upper limb vs. lower limb, with exception to the shoulder vs. pelvis. However, when muscles are included, the overall musculoskeletal network organization of the upper limb is strikingly different from that of the lower limb, particularly that of the more proximal structures of each limb. Importantly, the obtained data provide further evidence to be added to the vast amount of paleontological, gross anatomical, developmental, molecular and embryological data recently obtained that contradicts the long-standing dogma that the upper and lower limbs are serial homologues. In addition, the AnNA of the limbs of a trisomy 18 human fetus strongly supports Pere Alberch's ill-named "logic of monsters" hypothesis, and contradicts the commonly accepted idea that birth defects often lead to lower integration (i.e. more parcellation) of anatomical structures.

On the serial homology of the pectoral and pelvic girdles of tetrapods.

While fore- and hindlimbs are commonly assumed to be serially homologous, the serial homology of the pectoral and pelvic girdles is more ambiguous. We investigate the degree to which a common history, developmental program, and gene network are shared between the girdles relative to the rest of the appendicular skeleton. Paleontological data indicate that pectoral appendages arose millions of years before pelvic appendages. Recent embryological and genetic data suggest that the anatomical similarity between the fore- and hindlimbs arose through the sequential, derived deployment of similar developmental programs and gene networks, and is therefore not due to ancestral serial homology. Much less developmental work has however been published about the girdles. Here, we provide the first detailed review of the developmental programs and gene networks of the pectoral and pelvic girdles. Our review shows that, with respect to these programs and networks, there are fewer similarities between pelvic and pectoral girdles than there are between the limbs. The available data therefore support recent hypotheses that the anatomical similarities between the fore- and hindlimbs arose during the fin-to-limb transition through the derived co-option of similar developmental mechanisms, while the phylogenetically older pectoral and pelvic girdles have remained more distinct since their evolutionary origin.

Notch signaling induces cell proliferation in the labrum in a regulatory network different from the thoracic legs

The insect head is composed of several segments and an anterior non-segmental region. While patterning of the segmental region relies – at least in part – on the known trunk patterning mechanisms, development of the anterior most region remains poorly understood. The labrum is an enigmatic structure of the anterior median region (AMR) of the insect head. Based on similar development and gene expression patterns it has been suggested to be a serial homolog of trunk appendages. However, its position in the non-segmental region indicated an independent origin. In order to learn more about development of the AMR including the labrum, we screened the results of the large scale RNAi screen iBeetle to identify novel genes. We found the Notch ligand Tc-Serrate and the ubiquitin ligase Tc-mind bomb1 to be required for labrum formation. Further studies showed that Notch signaling is acting upstream of the genetic hierarchy and is required for regulating cell proliferation. We combined our work with previous data to compare the regulatory gene networks of labrum and trunk appendage formation. This reveals that despite the involvement of a similar set of genes, the genetic interactions are quite different.

Differential Expression of Ecdysone Receptor Leads to Variation in Phenotypic Plasticity across Serial Homologs.

Bodies are often made of repeated units, or serial homologs, that develop using the same core gene regulatory network. Local inputs and modifications to this network allow serial homologs to evolve different morphologies, but currently we do not understand which modifications allow these repeated traits to evolve different levels of phenotypic plasticity. Here we describe variation in phenotypic plasticity across serial homologous eyespots of the butterfly Bicyclus anynana, hypothesized to be under selection for similar or different functions in the wet and dry seasonal forms. Specifically, we document the presence of eyespot size and scale brightness plasticity in hindwing eyespots hypothesized to vary in function across seasons, and reduced size plasticity and absence of brightness plasticity in forewing eyespots hypothesized to have the same function across seasons. By exploring the molecular and physiological causes of this variation in plasticity across fore and hindwing serial homologs we discover that: 1) temperature experienced during the wandering stages of larval development alters titers of an ecdysteroid hormone, 20-hydroxyecdysone (20E), in the hemolymph of wet and dry seasonal forms at that stage; 2) the 20E receptor (EcR) is differentially expressed in the forewing and hindwing eyespot centers of both seasonal forms during this critical developmental stage; and 3) manipulations of EcR signaling disproportionately affected hindwing eyespots relative to forewing eyespots. We propose that differential EcR expression across forewing and hindwing eyespots at a critical stage of development explains the variation in levels of phenotypic plasticity across these serial homologues. This finding provides a novel signaling pathway, 20E, and a novel molecular candidate, EcR, for the regulation of levels of phenotypic plasticity across body parts or serial homologs.

Colour pattern homology and evolution in Vanessa butterflies (Nymphalidae: Nymphalini): eyespot characters.

Ocelli are serially repeated colour patterns on the wings of many butterflies. Eyespots are elaborate ocelli that function in predator avoidance and deterrence as well as in mate choice. A phylogenetic approach was used to study ocelli and eyespot evolution in Vanessa butterflies, a genus exhibiting diverse phenotypes among these serial homologs. Forty-four morphological characters based on eyespot number, arrangement, shape and the number of elements in each eyespot were defined and scored. Ocelli from eight wing cells on the dorsal and ventral surfaces of the forewing and hindwing were evaluated. The evolution of these characters was traced over a phylogeny of Vanessa based on 7750 DNA base pairs from 10 genes. Our reconstruction predicts that the ancestral Vanessa had 5 serially arranged ocelli on all four wing surfaces. The ancestral state on the dorsal forewing and ventral hindwing was ocelli arranged in two heterogeneous groups. On the dorsal hindwing, the ancestral state was either homogenous or ocelli arranged in two heterogeneous groups. On the ventral forewing, we determined that the ancestral state was organized into three heterogeneous groups. In Vanessa, almost all ocelli are individuated and capable of independent evolution relative to other colour patterns except for the ocelli in cells -1 and 0 on the dorsal and ventral forewings, which appear to be constrained to evolve in parallel. The genus Vanessa is a good model system for the study of serial homology and the interaction of selective forces with developmental architecture to produce diversity in butterfly colour patterns.

Appendage-patterning genes regulate male and female copulatory structures in horned beetles.

Explaining the extraordinarily rapid diversification of insect copulatory structures has been a longstanding objective in evolutionary biology. However, remarkably little is known about the developmental genetic underpinnings of their formation. Furthermore, recent work has questioned whether male genitalic structures in beetles are serially homologous to appendages, or even homologous to the genitalia of other orders. Using RNA interference, we demonstrate that several cardinal appendage-patterning genes regulate the formation of copulatory structures in Onthophagus beetles of both sexes. These results are in strong disagreement with previous findings in the model beetle species Tribolium castaneum, but congruent with earlier studies in true bugs and flies. Our results support the hypotheses that genitalic development is largely conserved across insect orders, and that genitalia constitute serial appendage homologues. Moreover, we identify two patterning genes with striking phenotypic effects in both sexes. In these cases, the affected structures are known to interact functionally during copulation, but are not homologous to each other. This suggests that shared developmental regulation of male and female copulatory structures may extend beyond components related by descent to those related by function.

The origin of a new fin skeleton through tinkering.

Adipose fins are positioned between the dorsal and caudal fins of many teleost fishes and primitively lack skeleton. In at least four lineages, adipose fins have evolved lepidotrichia (bony fin rays), co-opting the developmental programme for the dermal skeleton of other fins into this new territory. Here I provide, to my knowledge, the first description of lepidotrichia development in an adipose fin, characterizing the ontogeny of the redtail catfish, Phractocephalus hemioliopterus. Development of these fin rays differs from canonical lepidotrich development in the following four ways: skeleton begins developing in adults, not in larvae; rays begin developing at the fin's distal tip, not proximally; the order in which rays ossify is variable, not fixed; and lepidotrichia appear to grow both proximally and distally, not exclusively proximodistally. Lepidotrichia are often wavy, of irregular thickness and exhibit no regular pattern of segmentation or branching. This skeleton is among the most variable observed in a vertebrate appendage, offering a unique opportunity to explore the basis of hypervariation, which is generally assumed to reflect an absence of function. I argue that this variation reflects a lack of canalization as compared with other, more ancient lepidotrichs and suggest developmental context can affect the morphology of serial homologues.

Ptenidium pusillum (Gyllenhal, 1808) from egg to pupa (Coleoptera: Ptiliidae).

Eggs, larvae and pupae of Ptenidium pusillum obtained by rearing adults are described. Larval chaetotaxy is treated in detail. Two larval instars are identified, differing in minor chaetotaxic characters, pigmentation and measurements. The lack of urogomphi, confirmed in Ptenidium, is discussed in the context of current systematics of Ptiliidae. Serial chaetotaxic homology and between-instar homology are discussed. Observations related to biology of P. pusillum and associations with phoretic mites and nematodes are given.

The End of an Old Dogma with Crucial Implications for Medical and Biology Students and for Medicine: regenerative, Developmental, Paleontological and Evolutionary Studies Contradict the Fore‐hindlimb Serial Homology

Most evolutionary and medical textbooks state that the tetrapod fore and hindlimb are serial homologues. Here we show how regenerative studies of axolotls, developmental studies of tetrapods, and comparative and evolutionary studies of all major vertebrate groups, including recent re‐analyses of the appendicular muscles of chondrichthyans, dipnoans and coelacanths contradict this old dogma. The integrative analysis of the data available strongly supports the idea that the similarity of the muscles and bones of the fore and hindlimbs of tetrapods such as salamanders and modern humans is not due to serial homology, but is instead the result of independent evolutionary changes (homoplasy) occurred mainly during the origin of tetrapods due to the co‐option of similar genes for the development of both limbs. It also offers new insights about the ancestral Bauplan and morphogenetic gradients of tetrapod limbs, including the striking similarity of the zeugopodial (forearm/leg) and autopodial (hand/foot) muscles of the two limbs and ventro‐dorsal symmetry of the zeugopodial muscles of a same limb, about the marked differences between pelvic and pectoral girdle structures, the homeotic transformations related to the number/identity of the digits and associated soft tissue changes, and the differences between limb ontogeny and regeneration, and about limb birth defects and their crucial medical implications.

Capture of Prey, Feeding, and Functional Anatomy of the Jaws in Velvet Worms (Onychophora).

Onychophorans are carnivorous, terrestrial invertebrates that occur in tropical and temperate forests of the Southern Hemisphere and around the Equator. Together with tardigrades, onychophorans are regarded as one of the closest relatives of arthropods. One of the most peculiar features of onychophorans is their hunting and feeding behavior. These animals secrete a sticky slime, which is ejected via a pair of slime-papillae, to entangle the prey. After the prey has been immobilized, its cuticle is punctured using a pair of jaws located within the mouth. These jaws constitute internalized appendages of the second body segment and are innervated by the deutocerebrum; thus, they are homologous to the chelicerae of chelicerates, and to the (first) antennae of myriapods, crustaceans, and insects. The jaws are also serial homologs of the paired claws associated with each walking limb of the trunk. The structure of the jaws is similar in representatives of the two major onychophoran subgroups, the Peripatidae and Peripatopsidae. Each jaw is characterized by an outer and an inner blade; while the outer blade consists only of a large principal tooth and up to three accessory teeth, the inner blade bears numerous additional denticles. These denticles are separated from the remaining part of the inner jaw by a diastema and a soft membrane only in peripatids. The onychophoran jaws are associated with large apodemes and specialized muscles that enable their movement. In contrast to the mandibles of arthropods, the onychophoran jaws are moved along, rather than perpendicular to, the main axis of the body. Our elemental analysis reveals an increased incorporation of calcium at the tip of each blade, which might provide rigidity, whereas there is no evidence for incorporation of metal or prominent mineralization. Stability of the jaw might be further facilitated by the cone-in-cone organization of its cuticle, as each blade consists of several stacked, cuticular elements. In this work, we summarize current knowledge on the jaws of onychophorans, which are a characteristic feature of these animals.

Nymphalid eyespots are co-opted to novel wing locations following a similar pattern in independent lineages.

BackgroundVariation in the number of repeated traits, or serial homologs, has contributed greatly to animal body plan diversity. Eyespot color patterns of nymphalid butterflies, like arthropod and vertebrate limbs, are an example of serial homologs. These eyespot color patterns originated in a small number of wing sectors on the ventral hindwing surface and later appeared in novel wing sectors, novel wings, and novel wing surfaces. However, the details of how eyespots were co-opted to these novel wing locations are currently unknown.ResultsWe used a large data matrix of eyespot/presence absence data, previously assembled from photographs of contemporary species, to perform a phylogenetic investigation of eyespot origins in nine independent nymphalid lineages. To determine how the eyespot gene regulatory network acquired novel positional information, we used phylogenetic correlation analyses to test for non-independence in the origination of eyespots. We found consistent patterns of eyespot gene network redeployment in the nine lineages, where eyespots first redeployed from the ventral hindwing to the ventral forewing, then to new sectors within the ventral wing surface, and finally to the dorsal wing surface. Eyespots that appeared in novel wing sectors modified the positional information of their serial homolog ancestors in one of two ways: by changing the wing or surface identity while retaining sector identity, or by changing the sector identity while retaining wing and surface identity.ConclusionsEyespot redeployment to novel sectors, wings, and surfaces happened multiple times in different nymphalid subfamilies following a similar pattern. This indicates that parallel mutations altering expression of the eyespot gene regulatory network led to its co-option to novel wing locations over time.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0300-x) contains supplementary material, which is available to authorized users.

RNAi screening of developmental toolkit genes: a search for novel wing genes in the red flour beetle, Tribolium castaneum.

The amazing array of diversity among insect wings offers a powerful opportunity to study the mechanisms guiding morphological evolution. Studies in Drosophila (the fruit fly) have identified dozens of genes important for wing development. These genes are often called candidate genes, serving as an ideal starting point to study wing development in other insects. However, we also need to explore beyond the candidate genes to gain a more comprehensive view of insect wing evolution. As a first step away from the traditional candidate genes, we utilized Tribolium (the red flour beetle) as a model and assessed the potential involvement of a group of developmental toolkit genes (embryonic patterning genes) in beetle wing development. We hypothesized that the highly pleiotropic nature of these developmental genes would increase the likelihood of finding novel wing genes in Tribolium. Through the RNA interference screening, we found that Tc-cactus has a less characterized (but potentially evolutionarily conserved) role in wing development. We also found that the odd-skipped family genes are essential for the formation of the thoracic pleural plates, including the recently discovered wing serial homologs in Tribolium. In addition, we obtained several novel insights into the function of these developmental genes, such as the involvement of mille-pattes and Tc-odd-paired in metamorphosis. Despite these findings, no gene we examined was found to have novel wing-related roles unique in Tribolium. These results suggest a relatively conserved nature of developmental toolkit genes and highlight the limited degree to which these genes are co-opted during insect wing evolution.

Nymphalid eyespot serial homologues originate as a few individualized modules.

Serial homologues are repeated traits that share similar development but occur in different parts of the body. Variation in number of repeats accounts for substantial diversity in animal form and considerable work has focused on identifying the factors accounting for this variation. Little is known, however, about how serial homologues originally become repeated, or about the relative timing of repeat individuation relative to repeat origin. Here, we show that the serially repeated eyespots on nymphalid butterfly wings most likely arose as a small cluster of units on the ventral hindwing that were later co-opted to the dorsal and anterior wing surfaces. Based on comparative analyses of over 400 species, we found support for a model of eyespot origin followed by redeployment, rather than by the conventional model, where eyespots arose as a complete row of undifferentiated units that later gained individuation. In addition, eyespots most likely evolved from simpler pattern elements, single-coloured spots, which were already individuated among different wing sectors. Finally, the late appearance of eyespots on the dorsal, hidden wing surface further suggests that these novel complex traits originally evolved for one function (thwarting predator attacks) and acquired a second function (sexual signalling) when moved to a different body location. This broad comparative analysis illustrates how serial homologues may initially evolve as a few units serving a particular function and subsequently become repeated in novel body locations with new functions.

Redescription of late-instar larva of Ptinella aptera (Guérin-Méneville, 1839) (Coleoptera: Ptiliidae).

The late-instar larva of the featherwing beetle Ptinella aptera is redescribed. A coding system for chaetotaxic structures for ptiliid larvae is proposed and possible serial homology of setae across body segments is discussed. Previous, fragmentary and inaccurate descriptions of larval stages of P. aptera are discussed. The structures of immature P. aptera are compared with those of P. tenella and possible homologies and differences are indicated.

The origins of adipose fins: an analysis of homoplasy and the serial homology of vertebrate appendages

Adipose fins are appendages found on the dorsal midline between the dorsal and caudal fins in more than 6000 living species of teleost fishes. It has been consistently argued that adipose fins evolved once and have been lost repeatedly across teleosts owing to limited function. Here, we demonstrate that adipose fins originated repeatedly by using phylogenetic and anatomical evidence. This suggests that adipose fins are adaptive, although their function remains undetermined. To test for generalities in the evolution of form in de novo vertebrate fins, we studied the skeletal anatomy of adipose fins across 620 species belonging to 186 genera and 55 families. Adipose fins have repeatedly evolved endoskeletal plates, anterior dermal spines and fin rays. The repeated evolution of fin rays in adipose fins suggests that these fins can evolve new tissue types and increased structural complexity by expressing fin-associated developmental modules in these new territories. Patterns of skeletal elaboration differ between the various occurrences of adipose fins and challenge prevailing hypotheses for vertebrate fin origin. Adipose fins represent a powerful and, thus far, barely studied model for exploring the evolution of vertebrate limbs and the roles of adaptation and generative biases in morphological evolution.

Comparative anatomy, evolution, and homologies of tetrapod hindlimb muscles, comparison with forelimb muscles, and deconstruction of the forelimb-hindlimb serial homology hypothesis.

For more than two centuries, the idea that the forelimb and hindlimb are serially homologous structures has been accepted without serious question. This study presents the first detailed analysis of the evolution and homologies of all hindlimb muscles in representatives of each major tetrapod group and proposes a unifying nomenclature for these muscles. These data are compared with information obtained previously about the forelimb muscles of tetrapods and the muscles of other gnathostomes in order to address one of the most central and enigmatic questions in evolutionary and comparative anatomy: why are the pelvic and pectoral appendages of gnathostomes generally so similar to each other? An integrative analysis of the new myological data, combined with a review of recent paleontological, developmental, and genetic works and of older studies, does not support serial homology between the structures of these appendages. For instance, many of the strikingly similar forelimb and hindlimb muscles found in each major extant tetrapod taxon were acquired at different geological times and/or have different embryonic origins. These similar muscles are not serial homologues, but the result of evolutionary parallelism/convergence due to a complex interplay of ontogenetic, functional, topological, and phylogenetic constraints/factors.

Deconstructing the dogma of fore and hindlimb serial homology: evidence from regenerative, developmental, comparative, paleontological and evolutionary studies (919.3)

Most textbooks and papers state that the structures of the tetrapod fore‐ and hindlimb are serial homologues. We provide an updated discussion of this subject based on a literature review and on our regenerative studies of axolotls, developmental studies of tetrapods, and comparative and evolutionary studies of all major vertebrate groups, including recent re‐analyses of the appendicular muscles of chondrichthyans, dipnoans and coelacanths. The integrative analysis of the data available strongly supports the idea that the similarity of muscles and bones of the fore and hindlimbs of tetrapods such as salamanders and modern humans is not due to serial homology, but is instead the result of independent evolutionary changes (homoplasy) due to a complex interplay between developmental, functional, topological and phylogenetic constraints. It also offers new insights about the ancestral Bauplan and morphogenetic gradients of tetrapod limbs, including the striking similarity of the zeugopodial (forearm/leg) and autopodial (hand/foot) muscles of the two limbs and ventro‐dorsal symmetry of the zeugopodial muscles of a same limb, about the marked differences between pelvic and pectoral girdle structures, about homeotic transformations related to the number/identity of the digits and associated soft tissue changes, about limb birth defects, and about the differences between limb ontogeny and regeneration.Grant Funding Source: Faculty Start‐Up Package, Howard University College of Medicine

Wing serial homologs and the origin and evolution of the insect wing

The origin and evolution of insect wings has been the subject of extensive debate. The issue has remained controversial largely because of the absence of definitive fossil evidence or direct developmental evidence of homology between wings and a putative wing origin. Recent identification of wing serial homologs (WSHs) has provided researchers with a potential strategy for identifying WSHs in other species. Future comparative developmental analyses between wings and WSHs may clarify the important steps underlying the evolution of insect wings.

Origin and specification of the brain leucokinergic neurons of Drosophila: Similarities to and differences from abdominal leucokinergic neurons

The Drosophila central nervous system contains many types of neurons that are derived from a limited number of progenitors as evidenced in the ventral ganglion. The situation is much more complex in the developing brain. The main neuronal structures in the adult brain are generated in the larval neurogenesis, although the basic neuropil structures are already laid down during embryogenesis. The embryonic factors involved in adult neuron origin are largely unknown. To shed light on how brain cell diversity is achieved, we studied the early temporal and spatial cues involved in the specification of lateral horn leucokinin peptidergic neurons (LHLKs). Our analysis revealed that these neurons have an embryonic origin. We identified their progenitor neuroblast as Pcd6 in the Technau and Urbach terminology. Evidence was obtained that a temporal series involving the transcription factors Kr, Pdm, and Cas participates in the genesis of the LHLK lineage, the Castor window being the one in which the LHLKs neurons are generated. It was also shown that Notch signalling and Dimmed are involved in the specification of the LHLKs. Serial homologies with the origin and factors involved in specification of the abdominal leucokinergic neurons (ABLKs) have been detected.

Mature larva of Stenichnus collaris (Müller & Kunze) (Coleoptera: Staphylinidae: Scydmaeninae).

The mature larva of Stenichnus collaris is re-described on the basis of a shed larval skin. This is the first description of an immature Stenichnus identified by rearing to an adult beetle, and not only by collecting the larva in association with adults, as in previously published works. New data on the life history of St. collaris are provided, and possible serial homology of chaetotaxic structures across body segments is discussed. The structures of immature Nearctic St. turbatus, the only Stenichnus larva described with focus on the chaetotaxy, are compared with those of St. collaris and possible homologies are indicated.